Accepted Manuscript Incidence and Causes of Sudden Death in U.S. College Athletes Barry J. Maron, MD, FACC Tammy S. Haas, RN Caleb J. Murphy, BS Aneesha Ahluwalia, Stephanie Rutten-Ramos, DVM, PhD PII:
S0735-1097(14)01087-0
DOI:
10.1016/j.jacc.2014.01.041
Reference:
JAC 19881
To appear in:
Journal of the American College of Cardiology
Received Date: 13 November 2013 Revised Date:
15 January 2014
Accepted Date: 20 January 2014
Please cite this article as: Maron BJ, Haas TS, Murphy CJ, Ahluwalia A, Rutten-Ramos S, Incidence and Causes of Sudden Death in U.S. College Athletes, Journal of the American College of Cardiology (2014), doi: 10.1016/j.jacc.2014.01.041. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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INCIDENCE AND CAUSES OF SUDDEN DEATH IN U.S. COLLEGE ATHLETES
Short title: Sudden death in college athletes
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Barry J. Maron MD, FACC, Tammy S. Haas RN, Caleb J. Murphy BS, Aneesha Ahluwalia, Stephanie Rutten-Ramos DVM, PhD
Disclosures: none
Barry J. Maron, MD Hypertrophic Cardiomyopathy Center Minneapolis Heart Institute Foundation 920 East 28th Street, Suite 620 Minneapolis, MN 55407 Tel: 612-863-3996/Fax: 612-863-3875
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Corresponding Author:
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The Hypertrophic Cardiomyopathy Center, Minneapolis Heart Institute Foundation, Minneapolis, MN
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ABSTRACT
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Objectives. Reliably define the incidence and causes of sudden death in college student-athletes. Background. Frequency with which cardiovascular-related sudden death (SD) occurs in competitive athletes importantly impacts considerations for preparticipation screening strategies. Methods. We assessed databases (including autopsy reports) from both the U.S. National Sudden Death in Athletes Registry and National Collegiate Athletic Association (NCAA) (20022011). Results. Over the 10 year period, 182 SDs occurred (ages 20 ± 1.7; 85% males; 64% white): 52 resulting from suicide (n = 31) or drug abuse (n = 21), and 64 probably or likely attributable to cardiovascular causes (6/year). Of the 64 athletes, 47 had a confirmed post-mortem diagnosis (4/year), most commonly hypertrophic cardiomyopathy in 21, and congenital coronary anomalies in 8. The 4,052,369 athlete participations (in 30 sports over 10 years) incurred mortality risks of: suicide and drugs combined, 1.3/100,000 athlete-participation-years (5 deaths/year); and documented cardiovascular disease, 1.2/100,000 (4 deaths/year). Notably, cardiovascular deaths were 5-fold more common in African-American athletes than whites (3.8 vs. 0.7/100,000; p 30 years experience
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and expertise in this discipline (1,8,15-17). When necessary, autopsy findings were verified by communication with medical examiners. Detailed information on demographics, circumstances of death, and pertinent clinical data was assembled, sometimes from written accounts or telephone interviews with family members, witnesses or coaches.
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NCAA participation data
The NCAA is a governing body for colleges and universities with organized competitive athletic programs, comprising 1,273 member institutions, representing 85% of students
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competing in college. For 2002-2011, participation data was tabulated from the comprehensive NCAA Sports Sponsorship and Participation Rates Report (18), but which does not take into
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account the possibility of multi-sport participation. Demographic, gender and race/ethnic information were obtained from NCAA Student-Athlete Ethnicity Report (19). Comparison of data sources U.S. National Sudden Death in Athletes Registry (which primarily accesses public domain sources) and the internal NCAA Memorial Resolutions List were compared with respect to identification of sudden cardiovascular deaths in NCAA athletes. Of the 64 total SD cases on 4
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initial interrogation, the Registry method recognized 56 SDs (88%) including 14 not represented on the NCAA List. The NCAA included 50/64 cases (78%), including 8 not recognized by initial Registry searches, due to absence within the media reports of key words prospectively
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established for tracking these events (e.g., “athlete” or “sudden death”). Statistics
Mortality rates in NCAA athletes were compared to available data for suicide, drugs,
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drowning and cardiovascular causes in the general population: (1) U.S. National Vital Statistics Reports (20) with all causes of death for ages 15-24 years during 2006, the most recent year in
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which causes of mortality were tabulated according to age and race; (2) data reported for suicide in U.S. college students, ages 18-24 years, for 2009-2010 (21). Extent of one athlete-year was defined as participating in a sport from August to July.
Mortality rates were estimated by Poisson regression, and compared across populations
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and subpopulations. Mortality rates, incidence, and 95% confidence intervals were reported as deaths/100,000 athlete participation-years (or person-years). All analyses were performed in SAS 9.3 (SAS Institute; Cary, NC). Statistical significance was defined as p 0.2).
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Gender. Cardiovascular deaths were 6-fold more common in male than in female athletes (1.8/100,000 [95% CI: 0.3, 9.3] vs. 0.3/100,000 [95% CI: 0.2, 0.8]; p < 0.0001), but lower than the general male population of the same ages (2.8/100,000; 95% CI: 0.6, 14; p < 0.001). Suicide
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rate was 3-fold higher in males than females (1.1/100,000 [95% CI: 0.2, 5.8] vs. 0.3/100,000 [95% CI: 0.2, 0.8]; p < 0.01), but much lower than in the general male population of same age (16/100,000; p 2/100,000 do not include diagnostic autopsy or clinical
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data, i.e., Steinvil, et al. from Israel (6) and the Harmon, et al. study of U.S. college athletes (7). However, we wish to underscore that the differences in incidence of athletic field deaths
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between Harmon, et al. (7) and the present study are nevertheless relatively small when compared to the more compelling rates of SD due to the many other risks to living in the general population of the same age group (Figure 3). Indeed, an important aspect of the present investigation is the placing of cardiovascular SDs in college athletes within a broader context.
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Our analysis underscores the principle that NCAA athlete SDs represent a numerically low event rate phenonomen (1,3,6,9,11,15,23); for example, by comparison, annual automobile fatalities in the same age group are >2,500-fold more common. Furthermore, cardiovascular deaths in
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NCAA athletes are significantly less common than those in the general population but similar to the unexpectedly high combined suicide and drug-related mortality rates identified in these
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college athletes.
Notably, the cardiovascular SD rate in our college athletes is higher than that previously reported in a cohort of high school participants (1.2 vs. 0.7/100,000) (9). Although the determinants are uncertain, these differences are potentially attributable to the longer exposure by college student-athletes to rigid and rigorous training regimens extended over more substantial periods of life. SDs were, in fact, most common in Division I (scholarship) athletes 10
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for whom training and competition is most demanding. In addition, susceptibility to cardiovascular events could conceivably be influenced by risk factors associated with the initial experience of independent living at college, e.g., failure to adhere to healthy lifestyle practices
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with proper rest and nutrition, and increased exposure to alcohol and drugs. Such accessibility to drugs/alcohol in college athletes may be largely responsible for the higher SD rate compared to high school athletes (9).
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In a sizeable minority of athlete SDs, it was not possible to conclusively determine the cause of death, even after considering the submitted autopsy findings. This circumstance largely
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reflects the current state-of-the-art in the medical examiner community regarding the reliability for postmortem diagnoses in SDs due to genetic heart diseases (24,25). Indeed, a minority of our SD events (n = 17) were considered likely of cardiovascular origin, given the instantaneous collapse linked to physical exertion, even though a precise cause of death could not be assigned
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due to ambiguous or absent autopsy findings. Nevertheless, some of these latter deaths could have been due to non-cardiac causes, a potential source for over-estimating our SD rates. Alternatively, the small subset of athletes for whom diagnosis remains completely unresolved (n
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= 16) could possibly have included cardiovascular disease-related deaths and in this way underestimated SD incidence.
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Available estimates of the at-risk athlete population (i.e., the denominator) have limitations, given that we and other investigators (7) are obligated to use NCAA data expressed as participations, rather than for individual participants. With the possibility of multi-sport involvement by a small minority of athletes, there is the potential for overestimating the at-risk population, and thereby underestimating SD incidence.
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Also, in this regard, ion channelopathies (e.g., LQTS, Brugada syndrome, catecholaminergic polymorphic ventricular tachycardia), important but relatively uncommon causes of SD, are unlikely to be identified within a forensic-based registry such as ours due to the
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characteristic absence of structural cardiac abnormalities. This issue underscores the advantage of expert cardiac pathologist assessment of autopsy findings in SDs of young athletes or others (25). Certainly, the general level of expertise for cardiovascular pathology in the U.S. medical
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examiner community has been questioned (24).
African-American college athletes were at 5-fold greater risk for cardiovascular SD than
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white athletes (16). However, this SD rate in African-American athletes did not differ from the general population of the same age and race. For male athletes, mortality rates for cardiovascular disease, as well as suicide and drugs, exceeded that in female athletes (3 to 6fold), consistent with reports in other athlete populations (1,3,8,9,15,16). Determinants of such
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racial and gender differences remain unresolved.
Our data do not focus primarily on the current controvery regarding the most effective preparticipation screening strategy for detection of cardiovascular disease (2-7,10-15). However,
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certain inferences are unavoidable. In particular, our findings underscore the frequency and importance of false negative results whether screening is limited to history-taking and physical
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examination or includes a 12-lead ECG, i.e., the principle that not all at-risk athletes are detectable by screening (1,3,4,9,26). Based on autopsy confirmation of cause of death, about 60% of the athletes in our study cohort would probably have been identified by a screening 12lead ECG. However, we also estimate that at least 40% would likely have been “false negatives”, not reliably suspected by 12-lead ECGs, as part of broad-based screening initiatives in athletes (26). 12
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In conclusion, NCAA student-athletes do not appear to be at unique or particularly high risk for SD due to unsuspected cardiovascular disease. Furthermore, the relative importance of suicide and drug deaths reported here with respect to the health and safety of college athletes
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suggests there may be a disproportionate focus on cardiovascular disease in this population. These observations support the principle of enhanced resources and energy for suicide
prevention and control of drug use, as well as wider dissemination of automatic external
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defibrillators for secondary prevention of SD. Such initiatives may best serve the public health of
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college student-athletes.
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LEGENDS Figure 1. Comparative incidence of SD. Comparative incidence of SD due to cardiovascular disease (CV), suicide, or drugs in NCAA athletes 2001 to 2011, per 100,000 athlete participation-years.
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Figure 2. SDs in 166 NCAA athletes. Left: All causes. Right: Confirmed cardiovascular causes in 47 athletes. Symbols: † collapse virtually instantaneous during physical activity, suggesting underlying cardiovascular disease was responsible, in the absence of a firm post-mortem diagnosis. Abbreviations: AMI = acute myocardial infarction; ARVC = arrhythmogenic right ventricular cardiomyopathy; CAD = coronary artery disease; CM = cardiomyopathy; CV = cardiovascular; HCM = hypertrophic cardiomyopathy; LQTS = long QT syndrome; MVP = (myxomatous) mitral valve prolapse SCT = sickle cell trait. Not included here are 16 athletes in whom the cause of death remains completely unresolved.
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Figure 3. Causes of death in young people annually in U.S., including NCAA athletes. Reference citations are in parentheses. Symbols: * data for 15-24 year olds (20); †data available only for 8-39 year olds (15); ‡ estimated deaths in this age group, from National Weather Service (27); ɑ: average annual event rate for 15-24 year olds (28); β: average annual event rate for 16-25 year olds for all activities performed at time of event (29); Ω: average annual event rate for events involving survivors and non-survivors of all ages (30); ∆: age 12-22 years (17) Abbreviations: CV = cardiovascular; MN = Minnesota; NCAA = National Collegiate Athletic Association.
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REFERENCES 1.
Maron BJ. Sudden death in young athletes. N Engl J Med 2003;349:1064-1075.
2.
Corrado D, Basso C, Pavei A, et al. Trends in sudden cardiovascular death in young
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competitive athletes after implementation of a preparticipation screening program. JAMA 2006;296:1593-1601. 3.
Maron BJ, Thompson PD, Ackerman MJ, et al. Recommendations and considerations
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related to preparticipation screening for cardiovascular abnormalities in competitive athletes: Update 2007. Circulation 2007;115:1643-1655.
Chaitman BR. An electrocardiogram should not be included in routine preparticipation
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screening of young athletes. Circulation 2007;116:2610-2614. 5.
Myerburg RJ, Vetter VL. Electrocardiograms should be included in preparticipation screening of athletes. Circulation 2007;116:2616-2626.
Steinvil A, Chundadze T, Zeltser D, et al. Mandatory electrocardiographic screening of
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athletes to reduce their risk for sudden death proven fact or wishful thinking? J Am Coll Cardiol 2011;57:1291-1296.
Harmon KG, Asif IM, Klossner D, Drezner JA. Incidence of sudden cardiac death in
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national collegiate athletic association athletes. Circulation 2011;123:1594-1600. Maron BJ, Shirani J, Poliac LC, et al. Sudden death in young competitive athletes:
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Clinical, demographic and pathological profiles. JAMA 1996;276:199-204. 9.
Maron BJ, Haas TS, Ahluwalia A, Rutten-Ramos SC. Incidence of cardiovascular sudden deaths in Minnesota high school athletes. Heart Rhythm 2013;10:374-377.
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Corrado D, Pelliccia A, Bjørnstad HH, et al. Cardiovascular pre-participation screening of young competitive athletes for prevention of sudden death: proposal for a common European protocol. Eur Heart J 2005;26:516-524. Holst AG, Winkel BG, Theilade J, et al. Incidence and etiology of sports-related sudden
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cardiac death in Denmark--implications for preparticipation screening. Heart Rhythm 2010;10:365-371.
Thiene G, Corrado D, Schiavon M, Basso C. Screening of competitive athletes to
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prevent sudden death: Implement programmes now. Heart 2013;99:304-306. Drezner JA. ECG screening in athletes: time to develop infrastructure. Heart Rhythm
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2011;8:1560-1561. 14.
Corrado D, Pelliccia A, Heidbuchel H, et al. Recommendations for interpretation of 12lead electrocardiogram in the athlete. Eur Heart J 2010;31:243-259. Maron BJ, Doerer JJ, Haas TS, Tierney DM, Mueller FO. Sudden deaths in young
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competitive athletes: analysis of 1866 deaths in the United States, 1980-2006. Circulation 2009;119:1085-1092.
Maron BJ, Carney KP, Lever HM, et al. Relationship of race to sudden cardiac death in
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competitive athletes with hypertrophic cardiomyopathy. J Am Coll Cardiol 2003;41:974-
17.
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Harris KM, Haas TS, Eichner ER, Maron BJ. Sickle cell trait associated with sudden death in competitive athletes. Am J Cardiol 2012;110:1185-1188.
18.
DeHass DM. 1981-82-2007-2008 NCAA Sports Sponsorship and Participation Rates Report. Indianapolis, IN: NCAA; 2009.
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19.
Zgonc E. 1999-2000/2009-2010 NCAA Student-Athlete Ethnicity Report. Indianapolis, In: NCAA; 2010.
20.
Heron M, Hoyert DL, Murphy SL, et al. Deaths: final data for 2006. Natl Vital Stat Rep
21.
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2009;57:1-134.
Turner JC, Leno EC, Keller A. Causes or mortality among American college students: A pilot study. J Coll Student Psychother 2013;27:31-42.
Basso C, Thiene G, Mackey-Bojack S, et al. Myocardial bridging: A frequent component
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of the hypertrophic cardiomyopathy phenotype lacks systematic association with sudden
23.
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cardiac death. Eur Heart J 2009;30:1627-1634.
Maron BJ, Gohman TE, Aeppli D. Prevalence of sudden cardiac death during competitive sports activities in Minnesota high school athletes. J Am Coll Cardiol 1998;32:1881-1884.
Friedewald VE, Maron BJ, Roberts WC. The Editor’s Roundtable: Sudden death in
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athletes. Am J Cardiol 2007;100:1451-1459. 25.
Papadakis M, Ragu H, Behr ER, et al. Sudden cardiac death with autopsy findings of
26.
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uncertain significance. Circ Arrhythm Electrophysiol 2013;6:588-596. Rowin EJ, Maron BJ, Appelbaum E, et al. Significance of false negative
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electrocardiograms in preparticipation screening of athletes for hypertrophic cardiomyopathy. Am J Cardiol 2012;110:1027-1032. 27.
National Weather Service. Lightning Fatalities by State, 2002-2011. http://www.lightningsafety.noaa.gov/stats/02-11_deaths_by_state.pdf. Accessed 5/6/13.
28.
Centers for Disease Control and Prevention, National Center for Health Statistics. Multiple Cause of Death 2005-2006 on CDC WONDER On-line Database, released 17
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February 2010. Data are from the Multiple Cause of Death Files, 2005-2006, as compiled from data provided by the 57 vital statistics jurisdictions through the Vital Statistic Cooperative Program. Accessed at http://wonder.cdc.gov/mcd-icd 10-
29.
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archive2006lhtml on January 20, 2014.
Colorado Avalanche Information Center. Fatalities by Age, 1996-2006. Accessed at http://avalanche.state.co.us/wp-content/uploads/2013/09/Slide10.jpg on Jan 9, 2014.
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Maron BA, Haas TS, Maron BJ. Sudden death from collapsing sand holes. N Engl J
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Med 2007;356:2655-2656.
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30.
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Table 1. Sources Used to Identify Sudden Deaths in NCAA Athletes 1.
NCAA Memorial Resolutions List (compiled annually to recognize student-athletes
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who have died of any cause) LexisNexis archival informational database*
3.
News media accounts †
4.
Internet search engines (e.g., Google, Yahoo)
5.
Reports from U.S. Consumer Product Safety Commission (Washington, DC)
6.
Records of National Center for Catastrophic Sports Injury Research (U. North
7.
Reports directly to Registry‡
Symbols:
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Carolina, Chapel Hill, NC)
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2.
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* Access to authoritative news, legal, and public records (n = 5 billion searchable documents from thousands of sources)
† Assembled through Burrelle’s Informative Services (Livingston, NJ) with access to 18,000 U.S.
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newspapers and international media sources on a daily basis ‡ From physicians, attorneys, coroners/medical examiners, colleges, and patient advocacy/support
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organizations
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Table 2. Demographics and Causes of Death in 182 NCAA Student-Athletes
Race
No.
Age (y)
Male
Female White American
Suicide
31
19.9 ± 1.5
25
6
24
6
Drugs
21
20.1 ± 1.3
21
0
16
4
Confirmed/Presumed CV
64
20.2 ± 1.8
54
10
37
26
Confirmed CV
47
20.3 ± 1.9
41
6
22
24
Trauma
15
19.1 ± 1.4
13
2
13
Accidental drowning
11
19.8 ± 1.5
11
0
5
Sickle cell trait
11
19.7 ± 1.3
11
0
0
Heat stroke
5
19.8 ± 1.6
5
0
3
Brain aneurysm
3
20.0 ± 2
3
0
Pulmonary
3
19.7 ± 2.1
1
2
Sepsis
2
20.5 ± 0.7
1
1
Other 1
Sports*
football (10); track/CC (7); baseball (5); swimming (3)
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Cause of Death
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African-
NCAA Division
I
II
III
14
8
9
football (7); basketball (4); soccer (4); baseball (2)
10
5
6
1
basketball (23); football (16); soccer (8); track/CC (6)
33
14
17
1
basketball (19); football (11); soccer (5); swimming (4)
25
12
10
0
2
track/CC (5); football (3); lacrosse (2); swimming (2)
5
5
5
5
1
track/CC (4); soccer (3); baseball (2); basketball (1); football (1)
4
3
4
11
0
football (8); basketball (2); track (1)
8
2
1
2
0
football (3); baseball (1); basketball (1)
3
1
1
2
1
0
football (2); basketball (1)
0
2
1
1
2
0
basketball (2); football (1)
2
1
0
2
0
0
baseball (1); field hockey (1)
0
1
1
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1
20
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Totally unresolved
16
20.3 ± 2.4
9
7
13
3
0
football (5); track/CC (2); tennis (2); swimming (2)
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Abbreviations: CC = cross-country; CV = cardiovascular; NCAA = National Collegiate Athletic Association; y = years Symbols: * 4 most common sports shown
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Table 3. Mortality Rates in NCAA Athletes Compared to the General Population General Population
Deaths/100,000 athlete
Deaths/100,000
participation-years† No.
(95% CI)
person-years† (95% CI)
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Mortality category
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NCAA athletes 2002-2011
47
1.2 (0.8, 1.5)*
Confirmed/Presumed CV
64
1.6 (1.2, 2.0)*
Suicide
31
0.8 (0.5, 1.1)*α
9.8 (4.8, 19.8)
Drugs
21
0.5 (0.3, 0.8)
0.6 (0.3, 1.5)
Suicide/drugs combined
52
1.3 (1.0, 1.7)*
10.4 (6.0, 18.0)
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Confirmed CV
Accidental drowning‡
2.4 (2.2, 2.5)
11
0.3 (0.2, 0.5)*
1.5 (0.5, 5.0)
16
0.4 (0.2, 0.6)*
1.1 (0.4, 3.0)
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Unresolved
2.4 (2.2, 2.5)
Abbreviations: CI = confidence interval; CV = cardiovascular; NCAA = National Collegiate Athletic Association Symbols: * P
S0735-1097(14)01087-0
DOI:
10.1016/j.jacc.2014.01.041
Reference:
JAC 19881
To appear in:
Journal of the American College of Cardiology
Received Date: 13 November 2013 Revised Date:
15 January 2014
Accepted Date: 20 January 2014
Please cite this article as: Maron BJ, Haas TS, Murphy CJ, Ahluwalia A, Rutten-Ramos S, Incidence and Causes of Sudden Death in U.S. College Athletes, Journal of the American College of Cardiology (2014), doi: 10.1016/j.jacc.2014.01.041. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
INCIDENCE AND CAUSES OF SUDDEN DEATH IN U.S. COLLEGE ATHLETES
Short title: Sudden death in college athletes
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Barry J. Maron MD, FACC, Tammy S. Haas RN, Caleb J. Murphy BS, Aneesha Ahluwalia, Stephanie Rutten-Ramos DVM, PhD
Disclosures: none
Barry J. Maron, MD Hypertrophic Cardiomyopathy Center Minneapolis Heart Institute Foundation 920 East 28th Street, Suite 620 Minneapolis, MN 55407 Tel: 612-863-3996/Fax: 612-863-3875
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Corresponding Author:
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The Hypertrophic Cardiomyopathy Center, Minneapolis Heart Institute Foundation, Minneapolis, MN
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ABSTRACT
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Objectives. Reliably define the incidence and causes of sudden death in college student-athletes. Background. Frequency with which cardiovascular-related sudden death (SD) occurs in competitive athletes importantly impacts considerations for preparticipation screening strategies. Methods. We assessed databases (including autopsy reports) from both the U.S. National Sudden Death in Athletes Registry and National Collegiate Athletic Association (NCAA) (20022011). Results. Over the 10 year period, 182 SDs occurred (ages 20 ± 1.7; 85% males; 64% white): 52 resulting from suicide (n = 31) or drug abuse (n = 21), and 64 probably or likely attributable to cardiovascular causes (6/year). Of the 64 athletes, 47 had a confirmed post-mortem diagnosis (4/year), most commonly hypertrophic cardiomyopathy in 21, and congenital coronary anomalies in 8. The 4,052,369 athlete participations (in 30 sports over 10 years) incurred mortality risks of: suicide and drugs combined, 1.3/100,000 athlete-participation-years (5 deaths/year); and documented cardiovascular disease, 1.2/100,000 (4 deaths/year). Notably, cardiovascular deaths were 5-fold more common in African-American athletes than whites (3.8 vs. 0.7/100,000; p 30 years experience
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and expertise in this discipline (1,8,15-17). When necessary, autopsy findings were verified by communication with medical examiners. Detailed information on demographics, circumstances of death, and pertinent clinical data was assembled, sometimes from written accounts or telephone interviews with family members, witnesses or coaches.
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NCAA participation data
The NCAA is a governing body for colleges and universities with organized competitive athletic programs, comprising 1,273 member institutions, representing 85% of students
EP
competing in college. For 2002-2011, participation data was tabulated from the comprehensive NCAA Sports Sponsorship and Participation Rates Report (18), but which does not take into
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account the possibility of multi-sport participation. Demographic, gender and race/ethnic information were obtained from NCAA Student-Athlete Ethnicity Report (19). Comparison of data sources U.S. National Sudden Death in Athletes Registry (which primarily accesses public domain sources) and the internal NCAA Memorial Resolutions List were compared with respect to identification of sudden cardiovascular deaths in NCAA athletes. Of the 64 total SD cases on 4
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initial interrogation, the Registry method recognized 56 SDs (88%) including 14 not represented on the NCAA List. The NCAA included 50/64 cases (78%), including 8 not recognized by initial Registry searches, due to absence within the media reports of key words prospectively
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established for tracking these events (e.g., “athlete” or “sudden death”). Statistics
Mortality rates in NCAA athletes were compared to available data for suicide, drugs,
SC
drowning and cardiovascular causes in the general population: (1) U.S. National Vital Statistics Reports (20) with all causes of death for ages 15-24 years during 2006, the most recent year in
M AN U
which causes of mortality were tabulated according to age and race; (2) data reported for suicide in U.S. college students, ages 18-24 years, for 2009-2010 (21). Extent of one athlete-year was defined as participating in a sport from August to July.
Mortality rates were estimated by Poisson regression, and compared across populations
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and subpopulations. Mortality rates, incidence, and 95% confidence intervals were reported as deaths/100,000 athlete participation-years (or person-years). All analyses were performed in SAS 9.3 (SAS Institute; Cary, NC). Statistical significance was defined as p 0.2).
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Gender. Cardiovascular deaths were 6-fold more common in male than in female athletes (1.8/100,000 [95% CI: 0.3, 9.3] vs. 0.3/100,000 [95% CI: 0.2, 0.8]; p < 0.0001), but lower than the general male population of the same ages (2.8/100,000; 95% CI: 0.6, 14; p < 0.001). Suicide
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rate was 3-fold higher in males than females (1.1/100,000 [95% CI: 0.2, 5.8] vs. 0.3/100,000 [95% CI: 0.2, 0.8]; p < 0.01), but much lower than in the general male population of same age (16/100,000; p 2/100,000 do not include diagnostic autopsy or clinical
SC
data, i.e., Steinvil, et al. from Israel (6) and the Harmon, et al. study of U.S. college athletes (7). However, we wish to underscore that the differences in incidence of athletic field deaths
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between Harmon, et al. (7) and the present study are nevertheless relatively small when compared to the more compelling rates of SD due to the many other risks to living in the general population of the same age group (Figure 3). Indeed, an important aspect of the present investigation is the placing of cardiovascular SDs in college athletes within a broader context.
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Our analysis underscores the principle that NCAA athlete SDs represent a numerically low event rate phenonomen (1,3,6,9,11,15,23); for example, by comparison, annual automobile fatalities in the same age group are >2,500-fold more common. Furthermore, cardiovascular deaths in
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NCAA athletes are significantly less common than those in the general population but similar to the unexpectedly high combined suicide and drug-related mortality rates identified in these
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college athletes.
Notably, the cardiovascular SD rate in our college athletes is higher than that previously reported in a cohort of high school participants (1.2 vs. 0.7/100,000) (9). Although the determinants are uncertain, these differences are potentially attributable to the longer exposure by college student-athletes to rigid and rigorous training regimens extended over more substantial periods of life. SDs were, in fact, most common in Division I (scholarship) athletes 10
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for whom training and competition is most demanding. In addition, susceptibility to cardiovascular events could conceivably be influenced by risk factors associated with the initial experience of independent living at college, e.g., failure to adhere to healthy lifestyle practices
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with proper rest and nutrition, and increased exposure to alcohol and drugs. Such accessibility to drugs/alcohol in college athletes may be largely responsible for the higher SD rate compared to high school athletes (9).
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In a sizeable minority of athlete SDs, it was not possible to conclusively determine the cause of death, even after considering the submitted autopsy findings. This circumstance largely
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reflects the current state-of-the-art in the medical examiner community regarding the reliability for postmortem diagnoses in SDs due to genetic heart diseases (24,25). Indeed, a minority of our SD events (n = 17) were considered likely of cardiovascular origin, given the instantaneous collapse linked to physical exertion, even though a precise cause of death could not be assigned
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due to ambiguous or absent autopsy findings. Nevertheless, some of these latter deaths could have been due to non-cardiac causes, a potential source for over-estimating our SD rates. Alternatively, the small subset of athletes for whom diagnosis remains completely unresolved (n
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= 16) could possibly have included cardiovascular disease-related deaths and in this way underestimated SD incidence.
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Available estimates of the at-risk athlete population (i.e., the denominator) have limitations, given that we and other investigators (7) are obligated to use NCAA data expressed as participations, rather than for individual participants. With the possibility of multi-sport involvement by a small minority of athletes, there is the potential for overestimating the at-risk population, and thereby underestimating SD incidence.
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Also, in this regard, ion channelopathies (e.g., LQTS, Brugada syndrome, catecholaminergic polymorphic ventricular tachycardia), important but relatively uncommon causes of SD, are unlikely to be identified within a forensic-based registry such as ours due to the
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characteristic absence of structural cardiac abnormalities. This issue underscores the advantage of expert cardiac pathologist assessment of autopsy findings in SDs of young athletes or others (25). Certainly, the general level of expertise for cardiovascular pathology in the U.S. medical
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examiner community has been questioned (24).
African-American college athletes were at 5-fold greater risk for cardiovascular SD than
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white athletes (16). However, this SD rate in African-American athletes did not differ from the general population of the same age and race. For male athletes, mortality rates for cardiovascular disease, as well as suicide and drugs, exceeded that in female athletes (3 to 6fold), consistent with reports in other athlete populations (1,3,8,9,15,16). Determinants of such
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racial and gender differences remain unresolved.
Our data do not focus primarily on the current controvery regarding the most effective preparticipation screening strategy for detection of cardiovascular disease (2-7,10-15). However,
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certain inferences are unavoidable. In particular, our findings underscore the frequency and importance of false negative results whether screening is limited to history-taking and physical
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examination or includes a 12-lead ECG, i.e., the principle that not all at-risk athletes are detectable by screening (1,3,4,9,26). Based on autopsy confirmation of cause of death, about 60% of the athletes in our study cohort would probably have been identified by a screening 12lead ECG. However, we also estimate that at least 40% would likely have been “false negatives”, not reliably suspected by 12-lead ECGs, as part of broad-based screening initiatives in athletes (26). 12
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In conclusion, NCAA student-athletes do not appear to be at unique or particularly high risk for SD due to unsuspected cardiovascular disease. Furthermore, the relative importance of suicide and drug deaths reported here with respect to the health and safety of college athletes
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suggests there may be a disproportionate focus on cardiovascular disease in this population. These observations support the principle of enhanced resources and energy for suicide
prevention and control of drug use, as well as wider dissemination of automatic external
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defibrillators for secondary prevention of SD. Such initiatives may best serve the public health of
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college student-athletes.
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LEGENDS Figure 1. Comparative incidence of SD. Comparative incidence of SD due to cardiovascular disease (CV), suicide, or drugs in NCAA athletes 2001 to 2011, per 100,000 athlete participation-years.
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Figure 2. SDs in 166 NCAA athletes. Left: All causes. Right: Confirmed cardiovascular causes in 47 athletes. Symbols: † collapse virtually instantaneous during physical activity, suggesting underlying cardiovascular disease was responsible, in the absence of a firm post-mortem diagnosis. Abbreviations: AMI = acute myocardial infarction; ARVC = arrhythmogenic right ventricular cardiomyopathy; CAD = coronary artery disease; CM = cardiomyopathy; CV = cardiovascular; HCM = hypertrophic cardiomyopathy; LQTS = long QT syndrome; MVP = (myxomatous) mitral valve prolapse SCT = sickle cell trait. Not included here are 16 athletes in whom the cause of death remains completely unresolved.
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Figure 3. Causes of death in young people annually in U.S., including NCAA athletes. Reference citations are in parentheses. Symbols: * data for 15-24 year olds (20); †data available only for 8-39 year olds (15); ‡ estimated deaths in this age group, from National Weather Service (27); ɑ: average annual event rate for 15-24 year olds (28); β: average annual event rate for 16-25 year olds for all activities performed at time of event (29); Ω: average annual event rate for events involving survivors and non-survivors of all ages (30); ∆: age 12-22 years (17) Abbreviations: CV = cardiovascular; MN = Minnesota; NCAA = National Collegiate Athletic Association.
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Harmon KG, Asif IM, Klossner D, Drezner JA. Incidence of sudden cardiac death in
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Corrado D, Pelliccia A, Bjørnstad HH, et al. Cardiovascular pre-participation screening of young competitive athletes for prevention of sudden death: proposal for a common European protocol. Eur Heart J 2005;26:516-524. Holst AG, Winkel BG, Theilade J, et al. Incidence and etiology of sports-related sudden
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Maron BJ, Carney KP, Lever HM, et al. Relationship of race to sudden cardiac death in
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18.
DeHass DM. 1981-82-2007-2008 NCAA Sports Sponsorship and Participation Rates Report. Indianapolis, IN: NCAA; 2009.
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19.
Zgonc E. 1999-2000/2009-2010 NCAA Student-Athlete Ethnicity Report. Indianapolis, In: NCAA; 2010.
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Heron M, Hoyert DL, Murphy SL, et al. Deaths: final data for 2006. Natl Vital Stat Rep
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Basso C, Thiene G, Mackey-Bojack S, et al. Myocardial bridging: A frequent component
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of the hypertrophic cardiomyopathy phenotype lacks systematic association with sudden
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cardiac death. Eur Heart J 2009;30:1627-1634.
Maron BJ, Gohman TE, Aeppli D. Prevalence of sudden cardiac death during competitive sports activities in Minnesota high school athletes. J Am Coll Cardiol 1998;32:1881-1884.
Friedewald VE, Maron BJ, Roberts WC. The Editor’s Roundtable: Sudden death in
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Papadakis M, Ragu H, Behr ER, et al. Sudden cardiac death with autopsy findings of
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uncertain significance. Circ Arrhythm Electrophysiol 2013;6:588-596. Rowin EJ, Maron BJ, Appelbaum E, et al. Significance of false negative
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electrocardiograms in preparticipation screening of athletes for hypertrophic cardiomyopathy. Am J Cardiol 2012;110:1027-1032. 27.
National Weather Service. Lightning Fatalities by State, 2002-2011. http://www.lightningsafety.noaa.gov/stats/02-11_deaths_by_state.pdf. Accessed 5/6/13.
28.
Centers for Disease Control and Prevention, National Center for Health Statistics. Multiple Cause of Death 2005-2006 on CDC WONDER On-line Database, released 17
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February 2010. Data are from the Multiple Cause of Death Files, 2005-2006, as compiled from data provided by the 57 vital statistics jurisdictions through the Vital Statistic Cooperative Program. Accessed at http://wonder.cdc.gov/mcd-icd 10-
29.
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archive2006lhtml on January 20, 2014.
Colorado Avalanche Information Center. Fatalities by Age, 1996-2006. Accessed at http://avalanche.state.co.us/wp-content/uploads/2013/09/Slide10.jpg on Jan 9, 2014.
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Maron BA, Haas TS, Maron BJ. Sudden death from collapsing sand holes. N Engl J
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Med 2007;356:2655-2656.
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30.
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Table 1. Sources Used to Identify Sudden Deaths in NCAA Athletes 1.
NCAA Memorial Resolutions List (compiled annually to recognize student-athletes
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who have died of any cause) LexisNexis archival informational database*
3.
News media accounts †
4.
Internet search engines (e.g., Google, Yahoo)
5.
Reports from U.S. Consumer Product Safety Commission (Washington, DC)
6.
Records of National Center for Catastrophic Sports Injury Research (U. North
7.
Reports directly to Registry‡
Symbols:
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Carolina, Chapel Hill, NC)
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2.
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* Access to authoritative news, legal, and public records (n = 5 billion searchable documents from thousands of sources)
† Assembled through Burrelle’s Informative Services (Livingston, NJ) with access to 18,000 U.S.
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newspapers and international media sources on a daily basis ‡ From physicians, attorneys, coroners/medical examiners, colleges, and patient advocacy/support
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organizations
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Table 2. Demographics and Causes of Death in 182 NCAA Student-Athletes
Race
No.
Age (y)
Male
Female White American
Suicide
31
19.9 ± 1.5
25
6
24
6
Drugs
21
20.1 ± 1.3
21
0
16
4
Confirmed/Presumed CV
64
20.2 ± 1.8
54
10
37
26
Confirmed CV
47
20.3 ± 1.9
41
6
22
24
Trauma
15
19.1 ± 1.4
13
2
13
Accidental drowning
11
19.8 ± 1.5
11
0
5
Sickle cell trait
11
19.7 ± 1.3
11
0
0
Heat stroke
5
19.8 ± 1.6
5
0
3
Brain aneurysm
3
20.0 ± 2
3
0
Pulmonary
3
19.7 ± 2.1
1
2
Sepsis
2
20.5 ± 0.7
1
1
Other 1
Sports*
football (10); track/CC (7); baseball (5); swimming (3)
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Cause of Death
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African-
NCAA Division
I
II
III
14
8
9
football (7); basketball (4); soccer (4); baseball (2)
10
5
6
1
basketball (23); football (16); soccer (8); track/CC (6)
33
14
17
1
basketball (19); football (11); soccer (5); swimming (4)
25
12
10
0
2
track/CC (5); football (3); lacrosse (2); swimming (2)
5
5
5
5
1
track/CC (4); soccer (3); baseball (2); basketball (1); football (1)
4
3
4
11
0
football (8); basketball (2); track (1)
8
2
1
2
0
football (3); baseball (1); basketball (1)
3
1
1
2
1
0
football (2); basketball (1)
0
2
1
1
2
0
basketball (2); football (1)
2
1
0
2
0
0
baseball (1); field hockey (1)
0
1
1
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1
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Totally unresolved
16
20.3 ± 2.4
9
7
13
3
0
football (5); track/CC (2); tennis (2); swimming (2)
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Abbreviations: CC = cross-country; CV = cardiovascular; NCAA = National Collegiate Athletic Association; y = years Symbols: * 4 most common sports shown
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Table 3. Mortality Rates in NCAA Athletes Compared to the General Population General Population
Deaths/100,000 athlete
Deaths/100,000
participation-years† No.
(95% CI)
person-years† (95% CI)
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Mortality category
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NCAA athletes 2002-2011
47
1.2 (0.8, 1.5)*
Confirmed/Presumed CV
64
1.6 (1.2, 2.0)*
Suicide
31
0.8 (0.5, 1.1)*α
9.8 (4.8, 19.8)
Drugs
21
0.5 (0.3, 0.8)
0.6 (0.3, 1.5)
Suicide/drugs combined
52
1.3 (1.0, 1.7)*
10.4 (6.0, 18.0)
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Confirmed CV
Accidental drowning‡
2.4 (2.2, 2.5)
11
0.3 (0.2, 0.5)*
1.5 (0.5, 5.0)
16
0.4 (0.2, 0.6)*
1.1 (0.4, 3.0)
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Unresolved
2.4 (2.2, 2.5)
Abbreviations: CI = confidence interval; CV = cardiovascular; NCAA = National Collegiate Athletic Association Symbols: * P
